Disentangling confusions in inflorescence morphology: Patterns and diversity of reproductive shoot ramification in angiosperms

Terminology of inflorescence diversity has often been used in a confusing way in the literature, partly because it was based on uncritical and outdated definitions. In particular, the terms cyme, thyrse, and panicle have been misused. Although a more critical classification worked out by several authors is available, it is unfortunately not in general use because most of the relevant publications are written in German. In addition, some terms have not been used in the same way by morphologists and developmental geneticists. The present review attempts to remedy the situation with a simple outline of a classification based on: (i) different branching patterns; (ii) differential elongation of axes of different orders; and (iii) repetition of basic ramification patterns in different ways. Racemose and cymose branching are two extreme patterns; the former with limitation of axial orders to two, the second with limitation of lateral axes of each order to two. In a branching system, a sequence of racemose → cymose and, within the cyme, of dichasial → monochasial is common, but the reverse sequence generally does not occur. Systematic and evolutionary aspects of inflorescences are briefly discussed. Branching patterns are often stable in larger clades.Infiorescences of mutants studied in developmental genetic studies are mainly altered in flower or branch numbers or relative branch length, but not in branching patterns. This is also a contribution towards the goal of a unified terminology for the different fields of biology dealing with inflorescences.     

Towards an ontogenetic understanding of inflorescence diversity

Backgrounds and Aims

Conceptual and terminological conflicts in inflorescence morphology indicate a lack of understanding of the phenotypic diversity of inflorescences. In this study, an ontogeny-based inflorescence concept is presented considering different meristem types and developmental pathways. By going back to the ontogenetic origin, diversity is reduced to a limited number of types and terms.

Methods

Species from 105 genera in 52 angiosperm families are investigated to identify their specific reproductive meristems and developmental pathways. Based on these studies, long-term experience with inflorescences and literature research, a conceptual framework for the understanding of inflorescences is presented.

Key Results

Ontogeny reveals that reproductive systems traditionally called inflorescences fall into three groups, i.e. ‘flowering shoot systems’ (FSS), ‘inflorescences’ sensu stricto and ‘floral units’ (FUs). Our concept is, first, based on the identification of reproductive meristem position and developmental potential. The FSS, defined as a seasonal growth unit, is used as a reference framework. As the FSS is a leafy shoot system bearing reproductive units, foliage and flowering sequence play an important role. Second, the identification of two different flower-producing meristems is essential. While ‘inflorescence meristems’ (IMs) share acropetal primordia production with vegetative meristems, ‘floral unit meristems’ (FUMs) resemble flower meristems in being indeterminate. IMs produce the basic inflorescence types, i.e. compound and simple racemes, panicles and botryoids. FUMs give rise to dense, often flower-like units (e.g. heads). They occur solitarily at the FSS or occupy flower positions in inflorescences, rendering the latter thyrses in the case of cymose branching.

Conclusions

The ontogenetic concept differs from all existing inflorescence concepts in being based on meristems and developmental processes. It includes clear terms and allows homology statements. Transitional forms are an explicit part of the concept, illustrating the ontogenetic potential for character transformation in evolution.     

Inflorescence development in the Vitis–Ampelocissus clade of Vitaceae: the unusual lamellate inflorescence of Pterisanthes

Pterisanthes (Vitaceae) is a genus of c. 20 species of scandent climbers endemic to Southeast Asia with unusual lamellate inflorescences. Molecular phylogenetic analysis supports its relationship in the well‐supported Vitis–Ampelocissus–Nothocissus–Pterisanthes clade (i.e. the Ampelocissus–Vitis clade). Shoot tips and floral buds were collected from wild and greenhouse‐grown P. eriopoda at different developmental stages and were examined using epi‐illumination, light and scanning electron microscopy. Inflorescence and floral ontogeny was studied to discover how the lamellate inflorescence evolved and to make morphological comparisons to infer relationships with closely related members of Vitaceae. The second‐order branches in P. eriopoda are racemose and develop helically around the inflorescence axis in a similar fashion to Vitis and Ampelocissus. Inflorescence branching is restricted to the second order in P. eriopoda, whereas in Vitis and most Ampelocissus species subsequent branching orders culminate in the typical vitaceous determinate dichasium. In P. eriopoda subsequent lateral growth of the second‐order branches combined with the inhibition of peduncle or pedicel formation and loss of dichasial branching results in the unique lamellae in Pterisanthes, on which the floral primordia arise directly in a helical pattern. Floral development in P. eriopoda is the same as in other genera of Vitaceae examined to date with initiation of floral whorls centripetally, the calyx ring developing first and calyx lobes fused to cover the petals and stamen primordia. Given the recent phylogenetic results that placed Pterisanthes firmly within Ampelocissus, the most likely scenario is that the Pterisanthes inflorescence is derived from the thyrse of an Ampelocissus‐like ancestor and that the thyrse is a morphological synapomorphy of the Ampelocissus–Vitis clade. © 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, 179 , 725–741.     

5种甘草属植物花序和种子生产的位置效应及繁殖资源分配模式初步研究

以种植于新疆石河子的光果甘草( Glycyrrhiza glabra Linn.)、胀果甘草( G. inflata Batal.)、乌拉尔甘草( G. uralensis Fisch.)、黄甘草( G. eurycarpa P. C. Li)和蜜腺甘草( G. glabra var. glandulosa X. Y. Li)为研究对象,对植株不同部位的花序数量、花序正常发育率、每花序单花数量和果穗干质量,以及植株不同部位和花序不同部位的生物量投入比、座果率、结籽率、种子投影面积和种子千粒质量进行测定;在此基础上,对供试5种甘草属( Glycyrrhiza Linn.)植物的繁殖资源分配模式和种子生产策略进行分析。结果表明：同一植株内,光果甘草、乌拉尔甘草、黄甘草和蜜腺甘草的花序数量、花序正常发育率、每花序单花数量和果穗干质量从植株下部到上部总体上依次递减,而胀果甘草植株不同部位间这4项指标总体上无显著差异。同一植株内,胀果甘草植株中部的生物量投入比和座果率均较高,但其生物量投入比、座果率和结籽率在植株不同部位间均无显著差异;而供试另4种植物的生物量投入比、座果率和结籽率从植株下部到上部总体上依次递减。同一花序内,胀果甘草花序中部的生物量投入比明显高于花序上部和下部,座果率从花序下部到上部依次递减,结籽率则在花序不同部位间无显著差异,而供试另4种植物的生物量投入比、座果率和结籽率从花序下部到上部总体上依次递减。供试5种植物的种子投影面积和种子千粒质量在植株不同部位间和花序不同部位间均无显著差异。综合研究结果显示：在资源竞争、结构效应和花粉限制的影响下,供试5种甘草属植物存在2种不同的资源分配模式和种子生产格局。其中,光果甘草、乌拉尔甘草、黄甘草和蜜腺甘草通过减少对晚发育的花或果实的资源投入来保障早发育的花或果实获得较多的资源,达到繁殖成功的目的;而胀果甘草则采取对花和果实随机败育的方式减小资源竞争的压力,这2种繁殖资源分配模式和种子生产策略对提高甘草属植物的繁殖成功率具有重要作用。     

Comparative morphology and development of inflorescence adnation in rattan palms

The morphology and development of inflorescences in 14 genera and 52 species of rattans and related genera of Lepidocaryoid palms were examined. Inflorescences are free (not adnate) in Ancistrophyllum, Eremospatha and Oncocalamus. Adnation between the inflorescence and internode above occurs in Korthalsia, Myrialepis, Plectocomia and Plectocomiopsis. Adnation between the inflorescence and both the internode and leaf sheath above occurs in Calamus, Calospatha, Ceratolobus and Daemonorops. This leaf-borne, but initially axillary, bud is displaced on to the base of the next younger leaf primordium by the second plastochrone. Later elongation of the internode further separates the inflorescence from its original node. Stages of initiation and early development of adnate buds are illustrated for ten species. Vegetative buds of some Calamus species develop like inflorescence buds. However, other species have unusual bud positions which cannot be interpreted at present. The degree of inflorescence adnation tends to be greater in presumably specialized species than in unspecialized ones.     

Direct shoot regeneration from immature inflorescence cultures of <Emphasis Type="Italic">Chlorophytum arundinaceum</Emphasis> and <Emphasis Type="Italic">Chlorophytum borivilianum</Emphasis>

Direct shoot regeneration was achieved from immature inflorescence explants of Chlorophytum arundinaceum and C. borivilianum on half-strength Murashige & Skoog (MS) medium supplemented with 3.0 mg L⁻¹ BA, 150 mg L⁻¹ Ads, 0.1 mg L⁻¹ NAA and 3% (w/v) sucrose under a 16-h photoperiod. The shoot buds developed within 2–3 weeks of culture. High frequency of shoot bud regeneration was achieved when cultured on similar medium in subsequent subcultures. The apex portion (Type I) of the inflorescence produced more shoot buds as compared to the middle ones (type II). More than 75% of the terminal segment explants produced shoot buds within 4-week of culture. Response of basal portion (Type III) was negative for shoot bud initiation. Shoots rooted on half-strength basal MS medium supplemented with half-strength MS medium, 0.1 mg L⁻¹ IAA and 2% (w/v) sucrose. Micropropagated plantlets were hardened in the green house and successfully established in the soil where 90% of the plants survived. This protocol would be useful for commercial micropropagation and genetic improvement prograrmme.     

Developmental morphology of the shoot in Weddellina squamulosa and implications for shoot evolution in the Podostemaceae

BACKGROUND AND AIMS: In angiosperms, the shoot apical meristem produces a shoot system composed of stems, leaves and axillary buds. Podostemoideae, one of three subfamilies of the river-weed family Podostemaceae, have a unique 'shoot' that lacks a shoot apical meristem and is composed only of leaves. Tristichoideae have been interpreted to have a shoot apical meristem, although its branching pattern is uncertain. The shoot developmental pattern in Weddellinoideae has not been investigated with a focus on the meristem. Weddellinoideae are in a phylogenetically key position to reveal the process of shoot evolution in Podostemaceae. METHODS: The shoot development of Weddellina squamulosa, the sole species of Weddellinoideae, was investigated using scanning electron microscopy and semi-thin serial sections. KEY RESULTS: The shoot of W. squamulosa has a tunica-corpus-organized apical meristem. It is determinate and successively initiates a new branch extra-axillarily at the base of an immediately older branch, resulting in a sympodial, approximately plane branching pattern. Large scaly leaves initiate acropetally on the flanks of the apical meristem, as is usual in angiosperms, whereas small scaly leaves scattered on the stem initiate basipetally in association with the elongation of internodes. CONCLUSIONS: Weddellinoideae, like Tristichoideae, have a shoot apical meristem, leading to the hypothesis that the meristem was lost in Podostemoideae. The patterns of leaf formation in Podostemoideae and shoot branching in Weddellinoideae are similar in that these organs arise at the bases of older organs. This similarity leads to another hypothesis that the 'branch' in Weddellinoideae (and possibly Tristichoideae) and the 'leaf' in Podostemoideae are comparable, and that the shoot apical meristem disappeared in the early evolution of Podostemaceae.     

水稻幼穗形态发生与顶端分生组织的研究

应用“铸模”扫描电镜法和组织切片技术对水稻幼穗的形态发生过程和顶端分生组织（ Ａｐｉｃａｌｍ ｅｒｉｓｔｅｍ ）进行了系统而细致的研究。研究表明：从营养生长转入到生殖生长早期,水稻生长锥发生了显著的变化,根据苗端分生组织（ Ｓｈｏｏｔ ａｐｉｃａｌｍ ｅｒｉｓｔｅｍ , Ｓ Ａ Ｍ ）中原基分化的属性,将水稻幼穗早期起源和发育过程分为花序顶端分生组织期（ Ｉｎｆｌｏｒｅｓｃｅｎｃｅ ａｐｉｃａｌ ｍ ｅｒｉｓｔｅｍ ｐｈａｓｅ, Ｉ Ａ Ｍ Ｐ）、小穗顶端分生组织期（ Ｓｐｉｋｅｌｅｔ ａｐｉｃａｌ ｍ ｅｒｉｓｔｅｍ ｐｈａｓｅ, Ｓ Ｐ Ａ Ｍ Ｐ）、花顶端分生组织期（ Ｆｌｏｒａｌ ｍ ｅｒｉｓｔｅｍ ｐｈａｓｅ, Ｆ Ｍ Ｐ）。在这 ３ 个大的发育时期,又根据每一发育时期中的原基分生组织生长发育的程度及先后顺序分别又可分为：花序 ０ 期、花序Ⅰ期、花序Ⅱ期;小穗期Ⅰ期、小穗Ⅱ期、小穗Ⅲ期;内稃原基分化期、浆片原基分化期、雄蕊原基分化期、心皮原基分化期。同时,在研究过程中还发现了一些与前人所不同的形态发生特征,并初步探讨了水稻幼穗早期的起源及分化发育的机理。     

Patterns of angiospermy development before carpel sealing across living angiosperms: diversity,and morphological and systematic aspects

Almost all angiosperms are angiospermous, i.e. the ovules are enclosed in carpels at anthesis and during seed development, but angiospermy develops in different ways across angiosperms. The most common means of carpel closure is by a longitudinal ventral slit in carpels that are partly or completely free. In such carpels, the closure process commonly begins at midlength of the prospective longitudinal slit and then proceeds downward and upward. Closure by a transverse slit is rarer, but it is prominent in groups of the ANITA grade and in a few early branching monocots (some Alismatales) and some early branching eudicots (a few Ranunculaceae and Nelumbonaceae), in these eudicots combined with a more or less developed longitudinal slit. In all these cases the carpels have a single ovule in ventral median position. In ANITA lines with pluriovulate carpels, there is only a short longitudinal slit in the uniformly ascidiate carpels. In carpels with a unifacial style the closure area is narrow; this pattern is rare and scattered mainly in some wind‐pollinated monocots and eudicots. In most angiosperms the carpels become closed before the ovules are visible from the outside of the still incompletely closed carpels (early carpel closure). This is notably the case in the ANITA grade and magnoliids. Delayed carpel closure, with the ovules visible before the carpels are closed, is much rarer and is concentrated in a few monocots (mainly some Alismatales and some Poales) and a few eudicots (mainly a few Ranunculales and many Caryophyllales, and scattered in some other eudicots). A kind of delayed carpel closure (with the placenta visible before closure but mostly not the ovules) also occurs in syncarpous gynoecia with a free central placenta. Most gynoecia with a free central placenta occur in the superasterids. In such gynoecia the individual carpel tips are not differentiated but the opening in young gynoecia has the shape of a circular diaphragm. In this case, when ovary septa and free carpel tips are missing, the number of carpels is sometimes unclear (Primulaceae, Lentibulariaceae, some Santalaceae). Extremely ascidiate carpels are concentrated in the ANITA grade, a few magnoliids and some early branching monocots. Aspects of potential advantages of plicate vs. ascidiate carpels with regard to flexibility of pollen tube transmitting tract differentiation are discussed. © 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, 178 , 556–591.     

The effect of inflorescence display size and flower position on pollination success in two deceptive and one rewarding orchid

• Inflorescence display size and flower position on the inflorescence play important roles in plant reproduction, in the formation of fruits and are primarily linked to pollinator behaviour. We used three orchids to determine how visitation rates and choice of pollinator depend on number and position of the flowers along the inflorescence.
• We measured reproductive success in (1) natural conditions, (2) hand-pollination experiments and (3) an experimental design, by modifying composition of inflorescences in populations of two deceptive orchids, Orchis anthropophora and O. italica, and one rewarding orchid, Anacamptis coriophora subsp. fragrans.
• There were no differences in natural fruit production in relation to flower position on the inflorescence (i.e. upper versus lower part), suggesting no preference of pollinators for different parts of the inflorescence. Hand-pollination experiments highlighted low pollen limitation in A. coriophora subsp. fragrans but high limitation in O. italica and O. anthropophora. Reproductive success of deceptive orchids in experimental plots decreased significantly when flowers on the upper half of the inflorescence were removed leading to reduced floral display, while reproductive success of the nectariferous species did not differ significantly.
• Our data highlight that in the examined orchids there is no clear relationship between fruit formation and flower position along inflorescences. Thus we can affirm that, for orchids, the entire inflorescence plays a dominant role in insect attraction but the part of the flower spike does not influence the choice of the insect. This implies that all flowers have the same possibility of receiving visits from pollinators, and therefore each flower has the same opportunity to set fruit.

     

Intrapetiolar inflorescence buds in Salacca (Palmae): development and significance

The inflorescence in all species of Salacca is enclosed in a chamber within the leaf base and is exserted through a slit on the abaxial surface of the leaf base. The inflorescence bud is interpreted ds an axillary meristem that becomes radially displaced by adaxial growth of the leaf primordium. A fine channel is produced from the leaf axil to the base of the inflorescence and persists at maturity. The channel and the bud chamber enlarge as the leaf elongates. They are lined by an epidermal layer. There is no cellular breakdown until the collapse and tearing of tissues of the leaf during inflorescence enlargement late in ontogeny. The vegetative bud is positioned about 130⁰ from the axil of its subtending leaf and lies directly below the abaxial inflorescence slit of the leaf above. Vegetative bud development was not observed, hut there is a suggestion of relatively late initiation. The separation of. Eleiodoxa from Salacca is supported by differences in the development of inflorescence and vegetative buds.     

The origin, initiation and development of axillary shoot meristems in Lotus japonicus

BACKGROUND AND AIMS: Lotus japonicus 'Gifu' develops multiple axillary shoots in the cotyledonary node region throughout the growth of the plant. The origin, initiation and development of these axillary meristems were investigated. METHODS: Morphological, histological and mRNA in situ analyses were done to characterize the ontogeny of cotyledonary axillary shoot meristems in Lotus. Morphological characterization of a putative Lotus shoot branching mutant (super-accessory branches) sac, is presented. KEY RESULTS: By using expression of an L. japonicus STM-like gene as a marker for meristematic tissues, it was demonstrated that groups of cells maintained in the meristematic state at the cotyledonary axil region coincide with the sites where additional axillary meristems (accessory meristems) form. A Lotus shoot branching mutant, sac, is a putative Lotus branching mutant characterized by increased proliferation of accessory shoots in all leaf axils including the cotyledons. CONCLUSION: In Lotus, axillary shoot meristems continually develop at the cotyledonary node region throughout the growth of the plant. These cotyledonary primary and accessory axillaries arise from the position of a meristematic zone of tissue at the cotyledonary node axil region.     

The diversity and ontogenetic changes of phyllotaxis in wild-types and two leaf form mutants of Antirrhinum majus L.

We have analysed the phyllotactic patterns of the main shoot in vegetative and generative phases of growth in wild type and mutant plants of Antirrhinum majus L. Wild types 'Sippe50' and 'W l08' were compared to mutants grminifolia and phanlastica . The normal vegetative phyllotaxis of the wild type plants is decussate, but the inflorescence phyllotaxis is spiral and of the Fibonacci type. The phyllotaxis patterns of the mutants differ strongly from that of the wild type. Besides decussate phyllotaxis, whorls of three or four elements as well as spiral patterns in vegetative phase were observed. The vegetative phyllotaxis in mutants is ontogenetically unstable with frequent transitions between patterns, including the reversion of chirality of spiral phyllotaxis. The number of transitions per plant was larger in graminifolia than in phantastica . The inflorescence phyllotaxis was more stable and occasional non-typical phyllotaxis patterns finally transformed to a Fibonacci pattern. The results suggest a possible role of genetic factors in determining the regularity of spatial arrangement of organs.     

The effect of protandry on siring success in Chamerion angustifolium (Onagraceae) with different inflorescence sizes

Abstract Protandry, a form of temporal separation of gender within hermaphroditic flowers, may reduce the magnitude of pollen lost to selfing (pollen discounting) and also serve to enhance pollen export and outcross siring success. Because pollen discounting is strongest when selfing occurs between flowers on the same plant, the advantage of protandry may be greatest in plants with large floral displays. We tested this hypothesis with enclosed, artificial populations of Chamerion angustifolium (Onagraceae) by experimentally manipulating protandry (producing uniformly adichogamous or mixed protandrous and adichogamous populations) and inflorescence size (two-, six-, or 10-flowered inflorescences) and measuring pollinator visitation, seed set, female outcrossing rate, and outcross siring success. Bees spent more time foraging on and visited more flowers of larger inflorescences than small. Female outcrossing rates did not vary among inflorescence size treatments. However, seed set per fruit decreased with increasing inflorescence size, likely as a result of increased abortion of selfed embryos, perhaps obscuring the magnitude of geitonogamous selfing. Protandrous plants had a marginally higher female outcrossing rate than adichogamous plants, but similar seed set. More importantly, protandrous plants had, on average, a twofold siring advantage relative to adichogamous plants. However, this siring advantage did not increase linearly with inflorescence size, suggesting that protandry acts to enhance siring success, but not exclusively by reducing between-flower interference.     

Sex ratio and sex expression in an urban population of the silver moss,Bryum argenteum Hedw.

ABSTRACT

Introduction. A well-supported pattern among dioicous bryophytes is male rarity. However, few assessments of bryophyte sex ratios have been made across environmental gradients to assess the role of environment in shaping population sex ratios.

Methods. We systematically surveyed 200 shoots from a 20?m² urban population of Bryum argenteum, and regenerated each shoot apex until sex expression occurred (up to 315 days).

Key results. Female shoots outnumbered male shoots 132 to 68, giving a sex ratio of 1.94♀: 1♂. The female bias was found in two transects in higher light environments but not in the third transect, which had a lower light level and an equal sex ratio. Female shoots took longer than male shoots to reach gametangial induction (122 vs. 60 days) and longer to produce 5 inflorescences (120 vs. 80 days). Male shoots produced an average of 10× the total number of inflorescences compared to female shoots (34 vs. 3.5 inflorescences). Despite producing more inflorescences, male plants also produced more regenerant shoots, thus contradicting the prediction that a higher prefertilisation reproductive effort in males trades off with vegetative proliferation. Female plants harboured significantly more associated microbes than male plants.

Conclusions. Our results support the role of light in influencing sex ratios in this species, suggest that trade-offs between reproduction and vegetative growth may not be strong for males, and indicate a potential role of a sex-specific microbiome in influencing sex ratios.     

Behavioral and environmental determinants of reproductive success in traditional Moroccan Berber groups

The reproductive histories of women aged 45–70 years from a homogeneous Berber population of South Morocco were sampled from three contrasting environments: a small town (n = 75), villages in the lowlands (n = 217), and villages in the highlands (n = 128). The main reproductive variables oppose the relatively better conditions of fertile life in the lowlands to the more hostile ones in the highlands. Path analysis confirms this difference through reproductive behaviors and suggests the existence of mechanisms for controlling family size in town and in the rural lowlands, but not in the highlands. The estimates of survival function show significant differences among the three groups, the conditions for survival in the highlands being clearly less favorable. Rank tests of the association of survival data with several covariates indicate the association of survival data with vaccinations and with conditions of delivery. In spite of the lower rate of offspring survival, the highlander group would demonstrate a higher overall number of children reaching reproductive maturity, thanks to an extended reproductive span. © 1996 Wiley-Liss, Inc.